Abstract
Genic DNA functions are commonplace: coding for proteins and specifying non-messenger RNA structure. Yet most DNA in the biosphere is non-genic, existing in nuclei as non-coding or secondary DNA. Why so much secondary DNA exists and why its amount per genome varies over orders of magnitude (correlating positively with cell volume) are central biological problems. A novel perspective on secondary DNA function comes from natural eukaryote eukaryote chimaeras (cryptomonads and chlorarachneans) where two phylogenetically distinct nuclei have coevolved within one cell for hundreds of millions of years. By comparing cryptomonad species differing 13-fold in cell volume, we show that nuclear and nucleomorph genome sizes obey fundamentally different scaling laws. Following a more than 125-fold reduction in DNA content, nucleomorph genomes exhibit little variation in size. Furthermore, the present lack of significant amounts of nucleomorph secondary DNA confirms that selection can readily eliminate functionless nuclear DNA, refuting 'selfish' and 'junk' theories of secondary DNA. Cryptomonad nuclear DNA content varied 12-fold: as in other eukaryotes, larger cells have extra DNA, which is almost certainly secondary DNA positively selected for a volume-related function. The skeletal DNA theory explains why nuclear genome size increases with cell volume and, using new evidence on nucleomorph gene functions, why nucleomorph genomes do not.
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Selected References
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- Barnes K. L., Craigie R. A., Cattini P. A., Cavalier-Smith T. Chromatin from the unicellular red alga Porphyridium has a nucleosome structure. J Cell Sci. 1982 Oct;57:151–160. doi: 10.1242/jcs.57.1.151. [DOI] [PubMed] [Google Scholar]
- Cavalier-Smith T. Nuclear volume control by nucleoskeletal DNA, selection for cell volume and cell growth rate, and the solution of the DNA C-value paradox. J Cell Sci. 1978 Dec;34:247–278. doi: 10.1242/jcs.34.1.247. [DOI] [PubMed] [Google Scholar]
- Cavalier-Smith T. r- and K-tactics in the evolution of protist developmental systems: cell and genome size, phenotype diversifying selection, and cell cycle patterns. Biosystems. 1980;12(1-2):43–59. doi: 10.1016/0303-2647(80)90037-4. [DOI] [PubMed] [Google Scholar]
- Douglas S. E., Murphy C. A., Spencer D. F., Gray M. W. Cryptomonad algae are evolutionary chimaeras of two phylogenetically distinct unicellular eukaryotes. Nature. 1991 Mar 14;350(6314):148–151. doi: 10.1038/350148a0. [DOI] [PubMed] [Google Scholar]
- Forbes D. J., Kirschner M. W., Newport J. W. Spontaneous formation of nucleus-like structures around bacteriophage DNA microinjected into Xenopus eggs. Cell. 1983 Aug;34(1):13–23. doi: 10.1016/0092-8674(83)90132-0. [DOI] [PubMed] [Google Scholar]
- Friz C. T. The biochemical composition of the free-living amoebae Chaos chaos, Amoeba dubia and Amoeba proteus. Comp Biochem Physiol. 1968 Jul;26(1):81–90. doi: 10.1016/0010-406x(68)90314-9. [DOI] [PubMed] [Google Scholar]
- Gilson P. R., Maier U. G., McFadden G. I. Size isn't everything: lessons in genetic miniaturisation from nucleomorphs. Curr Opin Genet Dev. 1997 Dec;7(6):800–806. doi: 10.1016/s0959-437x(97)80043-3. [DOI] [PubMed] [Google Scholar]
- Gilson P. R., McFadden G. I. The miniaturized nuclear genome of eukaryotic endosymbiont contains genes that overlap, genes that are cotranscribed, and the smallest known spliceosomal introns. Proc Natl Acad Sci U S A. 1996 Jul 23;93(15):7737–7742. doi: 10.1073/pnas.93.15.7737. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hansmann P., Eschbach S. Isolation and preliminary characterization of the nucleus and the nucleomorph of a cryptomonad, Pyrenomonas salina. Eur J Cell Biol. 1990 Aug;52(2):373–378. [PubMed] [Google Scholar]
- Maier U. G., Hofmann C. J., Eschbach S., Wolters J., Igloi G. L. Demonstration of nucleomorph-encoded eukaryotic small subunit ribosomal RNA in cryptomonads. Mol Gen Genet. 1991 Nov;230(1-2):155–160. doi: 10.1007/BF00290663. [DOI] [PubMed] [Google Scholar]
- Maleszka R. Electrophoretic analysis of the nuclear and organellar genomes in the ultra-small alga Cyanidioschyzon merolae. Curr Genet. 1993 Dec;24(6):548–550. doi: 10.1007/BF00351721. [DOI] [PubMed] [Google Scholar]
- McFadden G. I., Gilson P. R., Douglas S. E., Cavalier-Smith T., Hofmann C. J., Maier U. G. Bonsai genomics: sequencing the smallest eukaryotic genomes. Trends Genet. 1997 Feb;13(2):46–49. doi: 10.1016/s0168-9525(97)01010-x. [DOI] [PubMed] [Google Scholar]
- Ohno S. So much "junk" DNA in our genome. Brookhaven Symp Biol. 1972;23:366–370. [PubMed] [Google Scholar]
- Orgel L. E., Crick F. H. Selfish DNA: the ultimate parasite. Nature. 1980 Apr 17;284(5757):604–607. doi: 10.1038/284604a0. [DOI] [PubMed] [Google Scholar]
- Petrov D. A., Chao Y. C., Stephenson E. C., Hartl D. L. Pseudogene evolution in Drosophila suggests a high rate of DNA loss. Mol Biol Evol. 1998 Nov;15(11):1562–1567. doi: 10.1093/oxfordjournals.molbev.a025883. [DOI] [PubMed] [Google Scholar]
- Rensing S. A., Goddemeier M., Hofmann C. J., Maier U. G. The presence of a nucleomorph hsp70 gene is a common feature of Cryptophyta and Chlorarachniophyta. Curr Genet. 1994 Nov-Dec;26(5-6):451–455. doi: 10.1007/BF00309933. [DOI] [PubMed] [Google Scholar]
